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Thermal Ablation of Lung Tumors: Focus on Microwave Ablation Thermoablation von Lungentumoren: Mikrowellenablation im Fokus Authors Thomas J. Vogl 1 , Nour-Eldin A. Nour-Eldin 1 , Moritz Hans Albrecht 1 , Benjamin Kaltenbach 1 , Wolfgang Hohenforst-Schmidt 2 , Han Lin 3 , Bita Panahi 1 , Kathrin Eichler 1 , Tatjana Gruber-Rouh 1 , Andrei Roman 1, 4 Affiliations 1 Institute for Diagnostic and Interventional Radiology, Goethe-Universitat Frankfurt am Main, Germany 2 Medical Clinic I, Fuerth’’ Hospital, Friedrich-Alexander- University Erlangen-Nurnberg, Fuerth, Germany 3 Department of Radiology and Radiological Sciences, Medical University of South Carolina, Charleston, United States 4 Department of Radiology, Iuliu Hatieganu University of Medicine and Pharmacy, Cluj-Napoca, Romania Key words ablation procedures, lung, metastases, NSCLC received 09.01.2017 accepted 27.03.2017 Bibliography DOI https://doi.org/10.1055/s-0043-109010 Published online: 16.5.2017 | Fortschr Röntgenstr 2017; 189: 828843 © Georg Thieme Verlag KG, Stuttgart · New York, ISSN 1438-9029 Correspondence Andrei Roman Department of Radiology, Iuliu Hatieganu University of Medicine and Pharmacy, Victor Babeş Nr. 8, 400012 Cluj-Napoca, Romania Tel.: +40/7 40/02 14 54 [email protected] ZUSAMMENFASSUNG Hintergrund Bild-gesteuerte thermische Ablationen können zur Behandlung von inoperablem primärem und metasta- tischem Lungenkrebs eingesetzt werden. Diese Techniken basieren auf der Erwärmung oder Abkühlung (Kryotherapie) eines Gewebevolumens um einen perkutanen Applikator, der eine Nekrose des Tumors induziert. Methode Die englischsprachige Literatur betreffend Ther- malablation der Lunge wurde durchgesehen. Die Radiofre- quenz-Ablation (RFA) ist das am weitesten verbreitete und erforschte Verfahren dieser Ablationstechniken. Die Mikro- wellenablation (MWA) stellt eine relativ neue Alternative dar, die unter gleichen Indikationen und in ähnlicher Weise wie die RFA durchgeführt wird. Es wurde experimentell und klinisch gezeigt, dass mittels MWA größere und sphärischere Ablationszonen über kürzere Zeiträume im Vergleich zu RFA erreicht werden können. In Europa und den USA stehen sieben verschiedene MWA-Systeme zur Verfügung, die signi- fikante Unterschiede in Größe und Form der erzeugten Abla- tionszonen aufweisen. Ergebnisse Die mit der MWA assoziierten Komplikationen, sowie deren Häufigkeiten, sind denen der RFA sehr ähnlich. Die lokalen Progressionsraten nach MWA von Lungentumoren variieren zwischen 0 % und 34 % die mit den Daten der RFA- Literatur vergleichbar sind. Schlussfolgerung Trotz technischer Verbesserungen hat die aktuelle Generation von MWA-Systemen ähnliche klinische Ergebnisse wie die RFA. Kernaussagen Bei der MWA handelt es ich um ein sicheres Therapiever- fahren welches daher als Behandlungsalternative bei nicht operablen Lungentumoren in Erwägung gezogen werden sollte. Da die Thermoablation von Lungentumoren immer mehr Anwendung findet, sollten Radiologen mit dem Erschei- nungsbild der Ablation in der Bildgebung vertraut sein. Obwohl die MWA theoretische Vorteile gegenüber der RFA hat, ist der Therapieerfolg vergleichbar. ABSTRACT Background Image-guided thermal ablation can be used for the treatment of medically inoperable primary and metastatic lung cancer. These techniques are based on the heating up or freezing (cryoablation) of a volume of tissue around a percu- taneous applicator that induces necrosis of the tumor. Method The English-language literature concerning thermal ablation of the lung was reviewed. Radiofrequency ablation (RFA) is the most widely performed and investigated of these techniques. Microwave ablation (MWA) represents a relatively new alternative that shares the same indications and is con- ducted in a very similar fashion as RFA. It has been experimen- tally and clinically shown that MWA produces larger, more spherical ablation zones over shorter periods of time compar- Review 828 Vogl TJ et al. Thermal Ablation ofFortschr Röntgenstr 2017; 189: 828843 This document was downloaded for personal use only. Unauthorized distribution is strictly prohibited.

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Page 1: Thermal Ablation of Lung Tumors: Focus on …...Thermal Ablation of Lung Tumors: Focus on Microwave Ablation Thermoablation von Lungentumoren: Mikrowellenablation im Fokus Authors

Thermal Ablation of Lung Tumors: Focus onMicrowave Ablation

Thermoablation von Lungentumoren:Mikrowellenablation im Fokus

Authors

Thomas J. Vogl1, Nour-Eldin A. Nour-Eldin1, Moritz Hans Albrecht1, Benjamin Kaltenbach1, Wolfgang Hohenforst-Schmidt2,

Han Lin3, Bita Panahi1, Kathrin Eichler1, Tatjana Gruber-Rouh1, Andrei Roman1, 4

Affiliations

1 Institute for Diagnostic and Interventional Radiology,

Goethe-Universitat Frankfurt am Main, Germany

2 Medical Clinic I, “Fuerth’’ Hospital, Friedrich-Alexander-

University Erlangen-Nurnberg, Fuerth, Germany

3 Department of Radiology and Radiological Sciences,

Medical University of South Carolina, Charleston, United

States

4 Department of Radiology, Iuliu Hatieganu University of

Medicine and Pharmacy, Cluj-Napoca, Romania

Key words

ablation procedures, lung, metastases, NSCLC

received 09.01.2017

accepted 27.03.2017

Bibliography

DOI https://doi.org/10.1055/s-0043-109010

Published online: 16.5.2017 | Fortschr Röntgenstr 2017; 189:

828–843 © Georg Thieme Verlag KG, Stuttgart · New York,

ISSN 1438-9029

Correspondence

Andrei Roman

Department of Radiology, Iuliu Hatieganu University of

Medicine and Pharmacy, Victor Babeş Nr. 8,400012 Cluj-Napoca, Romania

Tel.: +40/7 40/02 14 54

[email protected]

ZUSAMMENFASSUNG

Hintergrund Bild-gesteuerte thermische Ablationen können

zur Behandlung von inoperablem primärem und metasta-

tischem Lungenkrebs eingesetzt werden. Diese Techniken

basieren auf der Erwärmung oder Abkühlung (Kryotherapie)

eines Gewebevolumens um einen perkutanen Applikator, der

eine Nekrose des Tumors induziert.

Methode Die englischsprachige Literatur betreffend Ther-

malablation der Lunge wurde durchgesehen. Die Radiofre-

quenz-Ablation (RFA) ist das am weitesten verbreitete und

erforschte Verfahren dieser Ablationstechniken. Die Mikro-

wellenablation (MWA) stellt eine relativ neue Alternative dar,

die unter gleichen Indikationen und in ähnlicher Weise wie

die RFA durchgeführt wird. Es wurde experimentell und

klinisch gezeigt, dass mittels MWA größere und sphärischere

Ablationszonen über kürzere Zeiträume im Vergleich zu RFA

erreicht werden können. In Europa und den USA stehen

sieben verschiedene MWA-Systeme zur Verfügung, die signi-

fikante Unterschiede in Größe und Form der erzeugten Abla-

tionszonen aufweisen.

Ergebnisse Die mit der MWA assoziierten Komplikationen,

sowie deren Häufigkeiten, sind denen der RFA sehr ähnlich.

Die lokalen Progressionsraten nach MWA von Lungentumoren

variieren zwischen 0% und 34% die mit den Daten der RFA-

Literatur vergleichbar sind.

Schlussfolgerung Trotz technischer Verbesserungen hat die

aktuelle Generation von MWA-Systemen ähnliche klinische

Ergebnisse wie die RFA.

Kernaussagen▪ Bei der MWA handelt es ich um ein sicheres Therapiever-

fahren welches daher als Behandlungsalternative bei nicht

operablen Lungentumoren in Erwägung gezogen werden

sollte.

▪ Da die Thermoablation von Lungentumoren immer mehr

Anwendung findet, sollten Radiologen mit dem Erschei-

nungsbild der Ablation in der Bildgebung vertraut sein.

▪ Obwohl die MWA theoretische Vorteile gegenüber der

RFA hat, ist der Therapieerfolg vergleichbar.

ABSTRACT

Background Image-guided thermal ablation can be used for

the treatment of medically inoperable primary and metastatic

lung cancer. These techniques are based on the heating up or

freezing (cryoablation) of a volume of tissue around a percu-

taneous applicator that induces necrosis of the tumor.

Method The English-language literature concerning thermal

ablation of the lung was reviewed. Radiofrequency ablation

(RFA) is the most widely performed and investigated of these

techniques. Microwave ablation (MWA) represents a relatively

new alternative that shares the same indications and is con-

ducted in a very similar fashion as RFA. It has been experimen-

tally and clinically shown that MWA produces larger, more

spherical ablation zones over shorter periods of time compar-

Review

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ed to RFA. Seven different MWA systems are available in

Europe and the USA with significant differences in the size

and shape of the produced ablation zones.

Results The types of complications caused by MWA and their

rates of occurrence are very similar to those caused by RFA.

The local progression rates after MWA of lung malignancies

vary between 0% and 34% and are similar to those in the RFA

literature.

Conclusion Despite technical improvements, the current

generation of MWA systems has comparable clinical out-

comes to those of RFA.

Key Points▪ MWA is a safe technique that should be considered one

of the treatment options for medically inoperable lung

tumors

▪ As thermal ablations of lung tumors are becoming more

frequent, radiologists should be acquainted with the post-

ablation imaging characteristics

▪ Although MWA has some theoretical advantages over RFA,

the clinical outcomes are similar

Citation Format▪ Vogl TJ, Nour-Eldin NA, Albrecht MH et al. Thermal Abla-

tion of Lung Tumors: Focus on Microwave Ablation.

Fortschr Röntgenstr 2017; 189: 828–843

IntroductionThe curative treatment of lung tumors, both primary andmetastatic, has undergone substantial diversification in the lasttwo decades. New treatment techniques provide a range ofoptions from parenchyma-sparing surgical resection techniquesand video-assisted thoracoscopic surgery (VATS) to the highlyefficient radiation delivery method represented by stereotacticbody radiation therapy (SBRT) and image-guided thermal ablationtherapies, such as radiofrequency (RFA), microwave (MWA), andcryoablation. The multitude of techniques and their constantimprovement raise the question of which approach is most bene-ficial for optimal patient outcome. Although SBRT and the thermalablation therapies have shown lower control rates compared tosurgical resection, their main advantage is their reduced invasive-ness and impact on respiratory function. Therefore, they offerpatients with medically inoperable early-stage NSCLC or oligome-tastatic disease a potentially curative treatment option. Incomparison to RFA which has been in use since the early 2000 sand is currently the most widely performed and evaluated ther-mal ablation technique, MWA is a relatively new treatment option,with the first large patient series study being published in 2008 byWolf et al. [1]. Since then, more than 20 articles have beenpublished in the literature concerning the MW treatment ofNSCLC and lung metastases with a main focus on outcome andcomplications [2 – 22]. The purpose of this paper is to review theliterature regarding MWA in the broader context of thermal abla-tion. RFA and MWA are the most widely used techniques that arebased on inducing necrosis through high temperatures with bothprocedures performed in a similar fashion. Other techniques thatare used less often, such as cryoablation and irreversible electro-poration, will only be briefly discussed. The imaging follow-up,indications and some of the complications are identical betweenMWA and RFA. Therefore, complication management is based onthe more abundant RFA literature, with differences being high-lighted accordingly.

Technical considerationsMWA systems generate an ellipsoidal microwave field around aneedle-like applicator that is introduced into the tissue. Micro-waves are part of the electromagnetic spectrum with frequenciesbetween 300MHz and 300 GHz. Since water molecules have apositively and a negatively charged pole, they tend to align withthe electromagnetic waves. The oscillation of the electromagneticwave therefore causes a rapid flip motion of the water moleculeswhich results in heating of the adjacent tissue through themechanism of dielectric hysteresis. If the MW frequency perfectlymatched the molecule-specific resonance frequency of the watermolecules, all energy would be transformed into heat, but thepenetrability into the tissue would be low. The frequencies usedby the current MW manufacturers (915MHz and 2450MHz) onlypartially match the resonance frequency of the water moleculesand therefore assure efficient energy conversion into heat withsatisfactory tissue penetrability [23 – 25].

RFA is based on electromagnetic radio waves with frequenciesof less than 1MHz. An electric field is generated within the bodybetween the active applicator and a grounding pad (monopolarsystems) or between two electrodes located within the applicator.The alternating electric field, which is stronger in the vicinity ofthe applicator, induces the oscillation of ions, which, in turn, indu-ces frictional tissue heating. In contrast to MW, RF energy deposi-tion is dependent on the electrical permittivity of the tissue.Therefore, tissues with increased resistivity such as the aeratedlung have an insulating effect by limiting the transformation ofRF energy into heat energy to the close proximity of the applicator[26 – 28]. Although the vast majority of RFA ablations are per-formed percutaneously, bronchoscopy-guided RFA has also beenreported. This technique might lead to fewer complications suchas pneumothorax, but is limited by the need of having a bronchusin the close proximity of the tumor [29].

Cryoablation is a technique based on generating temperaturesas low as –160° C around an applicator that spread by convectionin the surrounding tissue. The ablation process lasts 25 – 30 min-utes and consists of successive freezing-thawing cycles whichinduce cell death by protein denaturation, membrane disruptionand microvascular thrombosis. The main advantage of cryoabla-

829Vogl TJ et al. Thermal Ablation of… Fortschr Röntgenstr 2017; 189: 828–843

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tion is better real-time CT monitoring of the ablation zone incomparison to the other techniques [28, 30, 31].

Irreversible electroporation (IRE) is the most recent ablationtechnique that induces cell death by irreversibly increasing thecell membrane permeability through the application of ahigh-voltage electrical field. General anesthesia is always neces-sary because of the neuromuscular blockade required to preventcurrent-induced muscular contractions. The utility of IRE in thetreatment of lung tumors remains to be proven [32].

Advantages of microwave ablationDespite the differences between MWA and RFA, both techniquesinduce coagulation necrosis of the tissue caused by temperaturesover 60◦C, even if the shape and size of the ablation zone, aswell as the speed at which the desired ablation volume is reacheddiffer between the two techniques. MWA generally produceslarger, more spherical and predictable ablation zones becausethe microwave field uniformly penetrates the tissue and is lessdependent on its properties. In contrast, RFA is hampered by thehigh electrical resistivity of lung tissue which limits energy deposi-tion. Tissue changes caused by ablation, such as carbonizationand desiccation, also increase tissue resistivity, thus further hin-dering the expansion of the ablation zone [33, 34]. The highelectrical resistivity of a ventilated lung and the ablation-inducedtissue inhomogeneity make the expansion of the ablation zoneparticularly reliant on thermal conduction, especially at its periph-ery. This fact renders the heat produced by RFA vulnerable tobeing washed out by vessels as small as 3mm, a phenomenonknown as the heat sink effect [35, 36]. In contrast, MWA, whoseheating deposition ability is favored by the presence of water,has been proven to be less susceptible to the heat sink effect byinducing complete thrombosis of most vessels with a diameter< 6mm [37, 38].

While discussing the performance of MWA, it should be takeninto account that seven different MWA systems are presently onthe European and American markets without considering thosethat are available only on Asian markets. The individual character-istics of these devices have been thoroughly described elsewhere[23, 24, 39]. These are either low-frequency (915MHz) or high-frequency (2450MHz) devices, with the maximum output powervarying between 32W and 140W and some of them allowing theconcomitant use of up to three antennas. The size and shape ofthe ablation zone created by MWA is most likely the complexresult of multiple factors such as the MW frequency, the designand cooling system of the antenna, the power setting and thetotal ablation time. The combination of these factors leads tosignificant differences between devices regarding the characteris-tics of the ablation zones (▶ Fig. 1). This has been demonstratedby Hoffmann et al. who directly compared four different MWAsystems under the same conditions using an ex-vivo liver model[40]. Therefore, upon deciding in favor of a specific MWA system,one should be well informed about its performance and how itcompares to the other devices on the market.

Ablation techniqueThermal ablation of a lung malignancy must be proposed to thepatient after prior consultation in an interdisciplinary tumorboard. The patient will be informed about alternative treatmentoptions while highlighting their advantages and disadvantages.Besides uncorrectable or severe coagulopathies, there is noabsolute contraindication regarding thermal ablation of lungtumors. Therefore, the coagulation status has to be verifiedbefore the intervention. Anticoagulation and antiplatelet drugshave to be ceased at least 5 days prior to the intervention. Thefollowing values are recommended by the consensus guidelinesfor the periprocedural management of coagulation status andhemostasis risk in percutaneous image-guided interventions:INR< 1.5; aPTT> 1.5x control if heparin is administered; and plate-let count> 50 000 [41].

The intervention may be performed under conscious sedationor general anesthesia. Hoffmann et al. concluded that neitherapproach was associated with different tumor control or compli-cation rates [42]. General anesthesia might prove useful foranxious patients or when multiple tumors are to be ablated duringthe same session. General anesthesia might also help when thetumor is located in the mobile lower segments of the lung, sincea longer breath-hold can be triggered by the anesthetist thusallowing more accurate targeting [42, 43]. At our institution,analgosedation using a combination of Piritramide and Diazepamadministered shortly before the intervention is preferred, withadditional administration of Piritramide if the need arises.

▶ Fig. 1 Example of ablation zones created by two different MWAsystems. a Ablation using a low-frequency (915MHz) MWA systemwith a duration of 10 minutes and a power of 45W. b Ablation usinga high-frequency (2450MHz) system with a duration of 8 minutesand an average power of 92W. Notice the difference between thesize and shape of the ablation zones.

▶ Abb. 1 Beispiel für Ablationszonen, die von zwei verschiedenenMWA-Systemen erzeugt wurden. a Ablation unter Verwendungeines niederfrequenten (915MHz) MWA-Systems mit einer Dauervon 10 Minuten und einer Leistung von 45W. b Ablation unter Ver-wendung eines Hochfrequenzsystems (2450MHz) mit einer Dauervon 8 Minuten und einer durchschnittlichen Leistung von 92W.Die Größe und Form der Ablationszonen variieren deutlich.

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The antenna insertion technique is almost identical to thatof CT-guided biopsies. Immediately prior to the intervention, anunenhanced CT scan of the chest is performed in order to planthe best puncture approach. Intravenous contrast agent mightsometimes be necessary in order to visualize intratumoral bloodvessels or to differentiate tumor from atelectasis. The patientposition will be chosen depending on the location of the lesion,but the prone position is recommended whenever possible, sinceit is associated with less chest wall motion. Lateral decubitusshould be avoided because of the unstable position and themore pronounced chest wall motion [44]. The antenna insertionpath should be chosen above the cranial margin of the rib andaway from higher caliber intrapulmonary blood vessels in orderto prevent intra-pleural and intra-parenchymatous bleeding.Crossing of lung fissures or emphysematous areas should also beavoided to prevent a pneumothorax. After choosing the bestpath, the skin entry point can be marked with the help of a metal-lic marker placed on the skin using single-slice scans. The punc-ture site will then be disinfected and isolated with sterile drapesand local anesthesia will be applied to the skin and pleura. Follow-ing a small skin incision using a scalpel, the antenna will be inser-ted under breath-hold as close as possible to the center of thetumor. Single-slice scans or CT fluoroscopy will be used to verifythe position of the antenna and to correct it if necessary [45– 47].

The success of the ablation depends mainly on the size of theablation margin which depends on the size of the tumor, the sizeof the ablation zone and the position of the antenna relative to thetumor. A tumor is likely to be successfully ablated if it is complete-ly engulfed by the ablation zone with a sufficiently wide safetymargin. The importance of the ablation margin has been provenafter thermal ablation of both the liver and the lung and mostauthors agree that an ablation margin of at least 5mm and, when-ever possible, up to 10mm is required for complete ablation [48 –52]. Therefore, as long as a sufficient ablation margin is achieved,it is not necessary for the antenna to be placed in the center of thetumor. However, larger tumors which often have an irregularshape, require a higher level of precision and might necessitatethe concomitant placement of multiple antennas or subsequentreablation [43]. Based mainly on the tumor size, but also on otherfactors such as the distance to the chest wall, mediastinum orlarge vessels, ablation time and power should be carefully adjus-ted in order to produce a large enough ablation zone withoutdoing unnecessary damage to the adjacent structures. As pre-viously discussed, the shape and size of the ablation zone is differ-ent between the various MWA devices and depends on the powersetting and duration of the ablation [40]. For each device, the rela-tionship between ablation time/power and the size of the ablationzone is documented and made available by the manufacturer.These parameters should be well known by the user because thetrue extent of the ablation zone often cannot be assessed on thescans performed during ablation. Despite the lower susceptibilityof MWA to the heat sink effect, it should not be ignored and high-er power settings or longer ablation times might be considered iflarger blood vessels are close to the tumor. Although it is a rareoccurrence, needle-tract seeding can be prevented by ablatingthe puncture tract while slowly removing the antenna after thetreatment is considered to be complete [17, 53, 54].

Imaging follow-upAs local ablative techniques become more widely used, radiolo-gists, even those not working in specialized centers, are more like-ly to encounter patients who have undergone such therapies andshould be familiar with the evolution of ablated lesions. The post-procedural evolution of the ablation zone is usually divided intothree continuous phases with corresponding histologic andimaging findings [55 – 57]. The features of the thermally ablatedlung tissue have first been described after RFA, but are similar tothose after MWA [37, 38].

The early phase (< 1 week)

The post-ablation histological and CT findings remain largelyunchanged over the first week [58]. The ablation zone isdescribed by most authors as a succession of three concentric lay-ers of tissue with different histological characteristics. The cells inthe innermost layer show signs of thermal damage but the tissuemaintains a seemingly intact alveolar structure. The middle layerhas a similar appearance as the inner one but the alveolar spacesare filled with effusion and some degree of congestion can benoticed. The outer layer shows strong congestion and hemor-rhage and consists of both damaged and viable cells [37, 58, 59].

On CT images acquired at this phase, the ablated lesionappears surrounded by an inner zone of ground glass opacity(GGO) which corresponds to the inner and middle histopathologi-cal layers and by a thin, dense outer rim which corresponds to theouter layer (▶ Fig. 1–4) [33, 55, 58, 59]. If contrast agent is admi-nistered, the outer rim usually shows circular benign periablation-al enhancement [60]. The ablated tumor is often still visible withinthe ablation zone but does not show any contrast enhancement.The ablation should be considered successful if the tumor iscompletely surrounded by the GGO and a sufficient ablationmargin was achieved. The outer hyperdense rim should not becounted as part of the completely ablated area as it might containviable cells. Incomplete ablation should be considered if thetumor exceeds the GGO and/or continues to show contrastenhancement [55, 58].

Non-contrast or contrast-enhanced CT should be performedwithin one day after ablation in order to evaluate the complete-ness of the ablation and to evaluate the potential necessity for anadditional procedure. The CT examination also allows for thedetection of early complications such as a broncho-pleural fistulathat might require a prolonged hospital stay.

The intermediate phase (1 week to 3 months)

During the first 2 – 3 months after the procedure, the necrotictissue within the ablation zone undergoes a process of granulationand fibrosis [57, 58]. As this process takes place, the GGO patterngradually changes into a nodular or fibrotic pattern while theablation zone steadily decreases in size. At this stage, the vastmajority of ablation zones will still exceed the size of the initialtumor. In some cases, it might stagnate in size and in other casesincrease in size over time, due to accompanying obstructive pneu-monitis (▶ Fig. 2) [58, 61]. Furthermore, the necrotic tissue maybe directly evacuated through a bronchus leading to the forma-

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tion of a cavity which has been shown to be related to anincreased risk of superinfection [1, 58, 62]. Most cavities disap-pear on follow-up, but some remain unchanged or even increasein size (▶ Fig. 2, 3) [57, 62, 63]. Completely ablated tumors willnormally not show contrast enhancement besides the persistingbenign periablational enhancement pattern [55]. Except for pro-

cedures in which a large part of the tumor remains unablated,local tumor progression will rarely be detected within the inter-mediate phase.

The late phase (> 3 months)

Three months after the procedure, the fibrous transformation isnearly complete, resulting in a stagnation or further decrease of

▶ Fig. 2 High-frequency ablation of a lung metastasis originating from a colorectal carcinoma (10 minutes; 96W). Typical evolution of the ablationzone after successful ablation. a Preinterventional aspect of the tumor. b Image obtained during ablation. Correct position of the antenna. c Imageobtained 24 hours after ablation showing the typical concentric rings. d Image obtained 3 months after ablation showing cavity formation, featureknown to be associated with a lack of progression. e Images obtained 7 months and f 16 months after ablation show continuous contraction of theablation zone.

▶ Abb. 2 Hochfrequenzablation einer Lungenmetastase eines kolorektalen Karzinoms (10 Minuten, 96W). Dargestellt ist die typische Entwicklungder Ablationszone nach erfolgreicher Ablation. a Präinterventioneller Aspekt des Tumors. b Die korrekte Position der Antenne wurde durch periin-terventionelle Bilder sicher gestellt. c Das Bild 24 Stunden nach der Ablation zeigte die typischen konzentrischen Ringe. d Das Bild 3 Monate nachder Ablation zeigte eine Hohlraumbildung. Dieses günstige Zeichen ist mit geringer bis keiner Progression assoziiert. e Die Bilder, die 7 Monate undf 16 Monate nach der Ablation acquiriert wurden, zeigen eine kontinuierliche Kontraktion der Ablationszone.

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the ablation zone (▶ Fig. 2– 4). At this point, the size can be smal-ler, larger or similar to that of the tumor prior to ablative treat-ment [64]. The pattern of the ablation zone can be fibrous, nodu-lar or cavitary [57]. The CT examination performed 3months afterthe ablation should be taken as a baseline for subsequent exami-nations and any further growth of the ablation zone should beconsidered as local progression [55, 64].

After 3 months, the ablation zone might show slight contrastenhancement which corresponds to a revascularization phenom-enon but it should remain weaker than the initial tumor enhance-ment [65]. The benign periablational enhancement might alsopersist for up to 6 months after the treatment [60].

▶ Fig. 3 High-frequency ablation of a pulmonary metastasis deriving from a colorectal carcinoma (8 minutes; 62W). Aspect of the tumor shortlybefore a and during ablation b. c Image obtained 24 hours after ablation showing a delayed pneumothorax that was successfully managed usingpleural drainage. After 3 months the ablation zone has a nodular aspect d, and there were changes into a cavity at 6 months e. f 9 months afterablation, the cavity is replaced by a fibrous pattern, but a new periablational nodularity can be noticed representing local progression of the tumor.

▶ Abb. 3 Hochfrequenzablation einer kolorektalen Lungenmetastase (8 Minuten, 62W). Gezeigt ist der Aspekt des Tumors kurz vor a und währendder Ablation b. c Das Bild, das 24 Stunden nach der Ablation akquiriert wurde, zeigte einen verzögerten Pneumothorax, der erfolgreich mit einerPleuradrainage behandelt wurde. Nach 3 Monaten hat die Ablationszone einen knotigen Aspekt d und wandelt sich nach 6 Monaten e in einenHohlraum um. f Neun Monate nach der Ablation wird der Hohlraum durch fibröses Gewebe ersetzt. Zusätzlich jedoch zeigte sich eine neue peria-blatorische Nodularität, die die lokale Progression des Tumors darstellt.

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PET/CT

PET/CT is a technique with the potential for improving the earlydetection of local tumor progression in certain situations. The18F-FDG-pattern immediately after successful ablation consists in

most cases of a high-uptake ring with central photopenia, butdiffuse or heterogeneous uptake might also be encountered(▶ Fig. 5) [66]. Three months after treatment, 57 – 68 % of theablation zones will show no or mild 18F-FDG uptake which has ahigh negative predictive value [67, 68]. In the remaining cases, a

▶ Fig. 4 High-frequency ablation of a lung metastasis originating from a colorectal carcinoma (6 minutes; 90W). Aspect of the tumor during a and24 hours after ablation b. c At 3months, the tumor has a nodular aspect. dOn a PET examination performed at 6 months, a hypermetabolic focus inthe ablation area is visualized (arrow), but because a concomitant CTshowed a decrease in size, no action was taken. The ablation zone continues toshrink until 9 months after ablation e and remains constant afterwards. f Two years after ablation, a fibrous pattern persists with no signs of localprogression.

▶ Abb. 4 Hochfrequenzablation einer kolorektalen Lungenmetastase (6 Minuten, 90W). Aspekt des Tumors während a und 24 Stunden nach derAblation b. c Nach 3 Monaten hatte der Tumor eine rundliche Erscheinung. d Bei einer PET-Untersuchung, die nach 6 Monaten durchgeführtwurde, wurde ein hypermetabolischer Fokus im Ablationsbereich detektiert (Pfeil), aber da eine simultane CT eine Größenregredienz zeigte, wurdekeine weitere Maßnahme getroffen. Die Ablationszone blieb weiterhin bis 9 Monate nach Ablation größenregredient e und danach konstant. f ZweiJahre nach der Ablation blieb ein fibröses Muster bestehen ohne Anzeichen lokaler Progression.

834 Vogl TJ et al. Thermal Ablation of… Fortschr Röntgenstr 2017; 189: 828–843

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moderate to high 18F-FDG uptake might persist. However, thisdoes not indicate progression on follow-up in the majority ofcases [68]. As the ablation zone undergoes fibrous transformationand shrinks, the ring-like uptake pattern that can still be presentat 6 months will be replaced by a nodular pattern. Therefore,6 months after treatment, a standardized uptake value (SUV)increase in the center of the ablation zone can appear withouthaving a pathological significance (▶ Fig. 4). After 12 months,the activity will usually be decreased [69]. Incomplete ablationshould be suspected when a high-uptake focus persists at thelocation of the tumor prior to ablation [66, 70]. Local progressionshould be considered when a new high-uptake focus is detectedwithin or at the periphery of the ablation zone after a period ofdecreased activity. An active region does not necessarily repre-sent tumoral tissue, especially in the first three months afterablation [61, 68, 69]. Additional ablation should be consideredby taking more factors into account, such as an increased size ofthe ablation zone, and the new occurrence of periablational nodu-larity or contrast enhancement patterns (▶ Fig. 3) [61, 69]. In thecase of doubt, biopsy of the suspicious focus can be performed[61]. In addition, reactively enlarged mediastinal lymph nodeswith increased 18F-FDG uptake are also likely to be encounteredwithin the first months after ablation, but should subside by12 moths [67, 71].

MRI

The MRI appearance of the ablation zone has been described bothon animal models as well as in a clinical setting in the previousdecade [72 – 75]. If not affected by artifacts, MRI offers goodvisualization with the same concentric rings aspect as seen onCT. Okuma et al. have shown that higher apparent diffusion coef-ficient values of the tumor measured three days after ablation canpredict complete ablation, but there are no other studies confirm-ing these findings [75]. MRI offers no clear advantages over CT

except for the lack of radiation, and because of its susceptibilityto artifacts and higher costs, MRI follow-up has not become partof the clinical routine in most centers.

Follow-up protocolTo date, there is no consensus regarding the ideal follow-upprotocol. Most authors employ a succession of enhanced or non-enhanced CT examinations with occasional or regular PET/CTexaminations [1, 2, 55, 56, 76]. At our institution, follow-up con-sists mostly of unenhanced CT scans. The first CT examination isperformed the day after ablation, not only to detect complica-tions, but also to evaluate whether the ablation was complete, oran additional ablation of the same tumor may be necessary. Thesecond CT examination is performed three months later with themain purpose of providing a baseline for the subsequent examina-tions which are performed in 3-month intervals within the firstyear and at 6-month intervals thereafter. PET/CTs are only em-ployed to confirm unclear cases of local progression.

Safety

Pain and chest wall damage

During the ablation of subpleural tumors, the heat expandsinto the surrounding tissue which is the cause of chest wall burns.Pain can be encountered after 2 – 27.6 % of MWA ablations(▶ Table 1) [1, 3, 8, 12]. Generally, the severity is mild to moder-ate, and it persists for a few days to a few weeks. Pain related toablative treatment usually responds well to analgesics, but casesof severe pain lasting up to a few months have also been reportedand can be attributed to intercostal neuralgia or pathologic ribfractures [17, 43]. Paramediastinal ablation can damage thephrenic nerves resulting in diaphragmatic paralysis with potentialserious impact on vital capacity [77]. The ablation of apicaltumors can lead to injury of the cervical plexus resulting in sen-sory and motor dysfunction [78]. In addition to nerve damage, asmall number of rib fractures and skin burns following MWA havealso been reported [1, 2, 7, 17]. Alexander et al. have shown thatRFA has a significantly higher risk of inducing rib fractures com-pared to MWA (15.9 % vs. 2.7 %) [7]. The induction of an artificialpneumothorax has been proposed as a safe method of preventingpain and chest wall damage [79].

Pneumothorax

The pneumothorax rates after MWA vary widely, ranging between8.5 – 63 % and are similar to those reported after RFA, rangingbetween 11% and 67% [1 – 3, 8, 9, 11, 12, 54, 80]. The high varia-bility of the reports is most likely a consequence of the thresholdchosen by the authors. The main cause for pneumothorax seemsto be associated with the insertion of the antenna and not withthe thermal effect of the ablation [81]. Therefore, the ablation ofmore than one tumor, very large or small tumors, and tumorslocated deep within the lung parenchyma that require multiplepleural punctures or antenna repositioning is associated with a

▶ Fig. 5 PET-CT aspect of the ablation zone 3 months after thetreatment with a typical high-uptake ring.

▶ Abb. 5 T-CT der Ablationszone 3 Monate nach der Behandlungmit typischer ringförmigen Glukoseanreicherung.

835Vogl TJ et al. Thermal Ablation of… Fortschr Röntgenstr 2017; 189: 828–843

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836 Vogl TJ et al. Thermal Ablation of… Fortschr Röntgenstr 2017; 189: 828–843

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higher risk of development of a pneumothorax. Tumors located inthe lower parts of the lungs (higher mobility), the traversal of lungfissures and lung emphysema, are also associated with anincreased pneumothorax risk [13, 54, 81, 82]. In most cases, thepneumothorax is small and does not require additional treatment.Between 0.8 – 15 % of ablations result in a large or progressivepneumothorax that requires placement of a drain [1 – 3, 8, 11 –13, 17, 22]. The occurrence of a pneumothorax may be particular-ly problematic if it appears before the definitive placement of theantenna. In this case, a new puncture can be attempted afterevacuating the air. The possibility of a delayed or recurrent pneu-mothorax that may require additional treatment also exists.Therefore, a chest radiography or CT is recommended within24 hours after ablation, since most pneumothoraces appearwithin this interval. Although rare, a significant pneumothoraxcan occur even later. Thus, it is crucial to inform patients and theirrelatives of this potential complication and the related symptoma-tology [2, 82, 83].

A broncho-pleural fistula is a complication caused by directcommunication between a bronchus and the pleural space. Itoccurs as a pneumothorax persisting despite the presence of achest drain. A fistula can become manifest during or shortly afterablation or it can appear in the weeks or months subsequent tothe treatment, as the necrotic tissue of a subpleural ablation isevacuated and a new communication is formed. This complica-tion is very rare and the treatment consists of pleurodesis,surgery, bronchoscopic management or a combination of these[13, 17, 54, 84].

Hemorrhage

A hemorrhage can occur by damaging an intrapulmonary orintercostal blood vessel. An intrapulmonary hemorrhage appearsas a rapidly expanding GGO starting from the antenna and canbe associated with hemoptysis. Intraparenchymal hemorrhagesoccur in 6 – 10 % of MWAs and lead to hemoptysis in 0 – 7 % ofcases [2, 3, 16, 22]. Yang et al. reported a hemoptysis rate ashigh as 36 % [12]. These rates have been reported to be higherafter RFA with 3 – 9 % resulting in hemoptysis and an almostdouble in hemorrhage [54]. Although the data are insufficient todraw a firm conclusion, the better results might be explained bythe lower susceptibility of MWA for the heat sink effect and astronger coagulative effect. Usually the hemorrhage is self-limit-ing and no action is needed except to carry on with the ablationwhich promotes coagulation. If the bleeding continues and isassociated with uncontrollable cough, one should react quicklyas heavy pulmonary bleeding might be lethal. The patient shouldbe positioned on the side of the ablation and hemostatic agentsshould be injected. A split intubation might be needed in orderto prevent asphyxia. In severe cases, only an embolization orexplorative thoracotomy is able to stop the bleeding [54, 76, 85].Damaging an intercostal vessel may result in a rapidly progressivehemothorax that usually requires endovascular or surgical treat-ment [54]. The best way to avoid hemorrhagic complications isto reconfirm that the patient has a safe coagulation profile and

to choose a puncture pathway that avoids intersecting largerblood vessels, especially in patients with high pulmonary bloodpressure [85].

Pleural effusion

Small asymptomatic pleural effusions are common after MWAand usually do not require treatment. They appear more often ifthe ablation is subpleural and are caused by an inflammatory reac-tion of the pleura [13, 86]. Large, symptomatic pleural effusionsoccur after 0 – 7.7 % of treatments and can be managed by inser-tion of a drain [12, 13, 16, 17, 22].

Infection

Postprocedural pneumonia is relatively common with ratesfollowing MWA ranging between 2 – 18 % [1, 11 – 13, 16, 17].The risk of pneumonia seems to be increased for patients whohave previously undergone radiotherapy [87]. Some authorsrecommend prophylactic antibiosis before and two days afterablation. In our institution, however, therapy is administered onlyin clinically manifest cases [13]. Lung abscess is another infectiousperiprocedural complication that can appear in 0.5 – 1.5 % ofcases [1, 13]. Patients with cavity formation, but also with emphy-sema have been reported to have an increased risk for abscess[1, 13, 87]. Both pneumonia and abscess should be regarded asserious complications that can result in procedure-related death[1, 87].

Other complications, such as pulmonary artery aneurysms andsystemic air embolisms, have been reported following RFA of lungtumors, but they are exceedingly rare [54].

Indications and outcome

NSCLC

Thermal ablation can be used with a curative intent only in stage INSCLC, because it cannot address lymph nodes directly and ithas a lower chance of success in complete ablation of tumorslarger than 3 cm [1, 2]. Given the better local control rates, thetreatment of choice for stage I NSCLC is considered to be eitheropen or video-assisted thoracic surgery [88]. However, in thecase of patients with early-stage NSCLC and severely impairedlung function, a local ablative therapy (SBRT or RFA) can be con-sidered [89].

Randomized controlled studies comparing radiotherapy (espe-cially SBRT) to thermal ablation therapies are currently not avail-able and most of the data regarding these techniques consist ofretrospective case series with low levels of evidence. A recentsystematic review and pooled analysis by Bi et al. compared theresults of RFA (328 patients) and SBRT (2767 patients) in thetreatment of stage I NSCLC [90]. The authors showed that thelocal control rates were significantly superior for SBRT comparedto RFA (1 year: 97% vs. 77%, 2 years: 92% vs. 48%, 3 years: 88%vs. 55 %, 5 years: 86 % vs. 42 %) even after correcting for tumorsize < 3 cm and age [90]. In 2015, Dupuy et al. published theresults of the American College of Surgeons Oncology Group

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Z4033 (Alliance) Trial which showed similar local control ratesafter RFA of stage IA NSCLC of 68.9 % at 1 year and 59.8 % at2 years and overall survival (OS) rates of 86.3 % at 1 year and69.8 % at 2 years [91]. Despite the lower local control rates forRFA compared to SBRT, there is no evidence for an increase inthe OS in either group as shown by the aforementioned pooledanalysis: The 1-, 2-, 3-, and 5-year OS rates for RFA were 85 %,67 %, 53% and 32%, respectively, whereas the OS rates for SBRTwere 85 %, 68 %, 56 % and 40 %, respectively [90]. These resultscan be explained by the overall poor condition of these patientsand by the possibility of a second ablation in the case of localprogression [91]. Likewise, based on an analysis of the Surveil-lance, Epidemiology, and End Results (SEER)/Medicare database(USA), Kwan et al. have shown that RFA has a lower OS comparedto sublobar resection of early-stage NSCLC in elderly patients,although this difference in OS was not significant when matchedfor demographic and clinical characteristics [92].

The ability of MWA to create larger, more spherical ablationzones, as well as the lower susceptibility to the heat sink effectshould theoretically lead to lower local progression rates (LPR).However, the patient series involving MWA treatment of stage INSCLC show similar outcomes with RFA. Liu et al. reported anLPR of 31 % (median follow-up of 12 months) while Yang et al.reported an LPR of 27.7 % (median follow-up 30 months), localcontrol rates at 1, 3 and 5 years of 96%, 64% and 48%, respective-ly, and OS rates at 1, 2 and 3 years of 89%, 63% and 43%, respec-tively [10, 12]. Similarly, Han et al. reported an LPR of 32% (medi-an follow-up 22 months) with local control rates at 1, 2 and3 years of 80.5 %, 74.8 % and 22.1 %, respectively, and cancer-specific survival rates at 1, 2 and 3 years of 95 %, 74% and 65%,respectively, (▶ Table 2) [15]. The other case series involvingMWA of NSCLC were either pooled together with metastases orinvolved locally advanced or metastatic NSCLC.

In the case of local progression after radiotherapy, reirradiationhas limited effectiveness in extending survival [93]. RFA and MWAhave been shown to prolong local tumor control and to alleviatesymptomatology in patients with local progression within theradiation field and therefore, if available, should be recommendedas a salvage therapy [21, 93, 94].

The currently accepted treatment for inoperable stage III andIV NSCLC consists of radiochemotherapy, but studies havesuggested that these patients might benefit from thermal abla-tion techniques. A randomized prospective study by Xu et al. com-pared the effectiveness of MWA vs. RT of the primary tumor inpatients with inoperable stage III NSCLC combined with chemo-therapy and RTof the lymph nodes. They reported lower radiationpneumonitis rates (3.9 % vs. 31.9 %) and a lower incidence ofprogressive disease in the MWA group (0 % vs. 17 %) [20]. Weiet al. compared the effectiveness of MWA and chemotherapy tochemotherapy alone and concluded that the MWA group had aprolonged progression-free survival compared to the chemother-apy-only group (10.9 months vs. 4.8 months) [19]. Both studiesshowed a tendency towards an improved OS that was, however,not statistically significant.

It has been shown that tissue heating increases the penetrationand retention of drugs co-administered at the time of ablation[95, 96]. The heat also has an immunomodulatory effect by

releasing intact antigens that can trigger an antitumor immuneresponse [97, 98]. Therefore, the size of the ablation zone can beenhanced by the concomitant local application of cytotoxic drugs[95, 99]. In a recent randomized study, Zhao et al. comparedthe intratumoral administration of 131I-labeled mouse/humanchimeric monoclonal antibodies against intracellular DNA com-bined with MWA to postoperative adjuvant chemoradiation ofstage II and III NSCLC. They found that the 1- and 2-year survivalrates of the MWA group were significantly better than those ofthe chemoradiation group [96]. The synergic effects of cytotoxicdrugs seem to be a promising approach to improve the results oflung thermal ablations, but more studies are required to provetheir utility in the clinical routine.

In brief, the survival rates of patients suffering from inoperableearly stage NSCLC treated with RFA or MWA do not show anysignificant difference compared to SBRT though the local controlrates seem to be inferior. Therefore, whenever available, bothtechniques should be discussed with the patient while highlight-ing their advantages and disadvantages. The thermal ablationtechniques can also be effectively employed as a salvage therapyafter unsuccessful RT and as a means of prolonging local tumorcontrol in stage III and IV NSCLC. Currently there is no evidencethat MWA is superior to RFA regarding local tumor control andoverall survival.

Metastases

Although the treatment concept of metastatic disease is usuallypalliative, patients with a controlled primary tumor and a limitednumber of metastases can be treated with a curative intent. Whenthe metastases are completely resected, 20 – 50% of patients mayreach long-time survival [100]. In the case of medically inoperablemetastases originating from a colorectal carcinoma, either SBRTor thermal ablation is recommended by the guidelines of theEuropean Society of Medical Oncology [101]. The largest andmost recent pooled analysis by the working group StereotacticRadiotherapy of the German Society for Radiation Oncology ana-lyzed the outcomes of 700 patients with lung oligometasticdisease treated with SBRT. They reported a 2-year local controlrate of 81.2 % and an OS rate of 54.4% (median follow-up of 14.3months) for up to 2 metastases treated per patient [102]. Similaroutcomes were observed in a systematic review analyzing 8 stud-ies with a total of 903 patients with lung metastases of colorectalorigin treated with thermal ablation. The local progression rateswere between 7% and 21% and the 1, 3 and 5-year survival ratesranged between 84 – 95 %, 35 – 72 % and 20 – 54%, respectively[103]. In a series of 566 patients with 1037 lung metastases treat-ed with RFA with a median follow-up of 35.5 months, De Baereet al. obtained 1-, 3-, and 5-year OS rates of 92 %, 67 % and51.5 %, respectively, with an LTP rate per patient of 18.1 %. Theyablated up to 4 metastases/patient with an average of 1.83 treat-ments/patient [80]. As prior research has suggested, thermal ab-lation techniques have very similar results with SBRT and there isno definitive proof for the superiority of one technique over theother. Accordingly, the latest ESMO colorectal carcinoma guide-line recommends that the treatment of oligometastatic diseaseshould be chosen from a ”toolbox” of procedures including ther-

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mal ablation therapies, SBRT and to a lesser extent chemoemboli-zation, while taking the patients preference, the size and locationof the metastases, technique invasiveness, local experience andother patient-related factors into account [101].

Thermal ablation has been shown not to affect respiratoryfunction in any way which might be an advantage over SBRT inpatients with severely limited lung function, especially when thetreatment of multiple lung metastases is planned [51, 91]. As anexample, Crombe et al. reported a patient who underwent RFA of23 lung metastases over a period of 10 years without loss ofrespiratory function [104].

Reports concerning MWA of lung metastases are still scarceand some are combined with series of NSCLC. Vogl et al. reporteda local progression rate of 26.9 % (mean follow-up of 10 months)in a series of 130 ablated lung metastases. The 1- and 2-year OSrates were 91.3 % and 75 %, respectively [2]. Lu et al. reportedmuch worse 1-, 2-, and 3-year OS rates after the ablation of 37lung metastases: 47.6 %, 23.8 %, and 14.3 %, respectively [3].Finally, Egashira et al. reported an LTP of only 2.3 % after the abla-tion of 87 lung metastases with a median follow-up of 15 months[22]. The small number of studies concerning lung metastases aswell as the high variability of the reported results and methods donot allow a satisfactory comparison of MWA to the previouslydiscussed techniques (▶ Table 2).

ConclusionMWA is a relatively new thermal ablation technique with increas-ing use in the treatment of inoperable lung tumors. MWA has sim-ilar complication rates with RFA and, therefore, can be regarded asa safe technique. Initial experimental animal models have shownclear advantages of MWA over RFA. MWA creates larger, morespherical and less time-consuming ablation zones and is less sus-ceptible to the heat sink effect. However, the relatively few andheterogeneous studies concerning MWA do not provide sufficientevidence to indicate any advantage in local control or overallsurvival compared to RFA. A larger body of evidence includingrandomized controlled trials is necessary to prove if the technicaladvantages of MWA translate into improved clinical outcomescompared to RFA.

CLINICAL RELEVANCE OF THE STUDY

▪ Thermal ablation and SBRT are currently the main curative

treatment options for medically inoperable lung tumors.

▪ Despite a slightly lower local control rate for thermal abla-

tion, there is no evidence for a difference in survival rates

between thermal ablation and SBRT.

▪ MWA has some theoretical advantages over RFA, but the

complications and clinical outcomes are similar.

Conflict of Interest

The authors declare that they have no conflict of interest.

References

[1] Wolf FJ, Grand DJ, Machan JT et al. Microwave Ablation of Lung Malig-nancies: Effectiveness, CT Findings, and Safety in 50 Patients. Radiology2008; 247: 871–879

[2] Vogl TJ, Naguib NN, Gruber-Rouh T et al. Microwave ablation therapy:clinical utility in treatment of pulmonary metastases. Radiology 2011;261: 643–651

[3] Lu Q, CaoW, Huang L et al. CT-guided percutaneous microwave ablationof pulmonary malignancies: Results in 69 cases. World journal of surgicaloncology 2012; 10: 80

[4] Carrafiello G, Mangini M, Fontana F et al. Complications of microwaveand radiofrequency lung ablation: personal experience and review of theliterature. La Radiologia medica 2012; 117: 201–213

[5] Wolf FJ, Aswad B, Ng T et al. Intraoperative microwave ablation of pul-monary malignancies with tumor permittivity feedback control: ablationand resection study in 10 consecutive patients. Radiology 2012; 262:353–360

[6] Vogl TJ, Worst TS, Naguib NN et al. Factors influencing local tumor con-trol in patients with neoplastic pulmonary nodules treated with micro-wave ablation: a risk-factor analysis. American journal of roentgenology2013; 200: 665–672

[7] Alexander ES, Hankins CA, Machan JT et al. Rib fractures after percuta-neous radiofrequency and microwave ablation of lung tumors: incidenceand relevance. Radiology 2013; 266: 971–978

[8] Belfiore G, Ronza F, Belfiore MP et al. Patients' survival in lung malignan-cies treated by microwave ablation: our experience on 56 patients.European journal of radiology 2013; 82: 177–181

[9] Carrafiello G, Mangini M, Fontana F et al. Microwave ablation of lungtumours: single-centre preliminary experience. La Radiologia medica2014; 119: 75–82

[10] Liu H, Steinke K. High-powered percutaneous microwave ablation ofstage I medically inoperable non-small cell lung cancer: a preliminarystudy. Journal of medical imaging and radiation oncology 2013; 57:466–474

[11] Wei Z, Ye X, Yang X et al. Microwave ablation in combination with che-motherapy for the treatment of advanced non-small cell lung cancer.Cardiovascular and interventional radiology 2015; 38: 135–142

[12] Yang X, Ye X, Zheng A et al. Percutaneous microwave ablation of stage Imedically inoperable non-small cell lung cancer: clinical evaluation of47 cases. Journal of surgical oncology 2014; 110: 758–763

[13] Zheng A, Wang X, Yang X et al. Major complications after lung micro-wave ablation: a single-center experience on 204 sessions. The Annalsof thoracic surgery 2014; 98: 243–248

[14] Acksteiner C, Steinke K. Percutaneous microwave ablation for early-stage non-small cell lung cancer (NSCLC) in the elderly: a promisingoutlook. Journal of medical imaging and radiation oncology 2015; 59:82–90

[15] Han X, Yang X, Ye X et al. Computed tomography-guided percutaneousmicrowave ablation of patients 75 years of age and older with early-stage nonsmall cell lung cancer. Indian journal of cancer 2015; 52(Suppl. 2): e56–e60

[16] Ni X, Han JQ, Ye X et al. Percutaneous CT-guided microwave ablation asmaintenance after first-line treatment for patients with advancedNSCLC. OncoTargets and therapy 2015; 8: 3227–3235

[17] Splatt AM, Steinke K. Major complications of high-energy microwaveablation for percutaneous CT-guided treatment of lung malignancies:Single-centre experience after 4 years. Journal of medical imaging andradiation oncology 2015; 59: 609–616

[18] Sun YH, Song PY, Guo Y et al. Computed tomography-guided percuta-neous microwave ablation therapy for lung cancer. Genetics and mole-cular research: GMR 2015; 14: 4858–4864

840 Vogl TJ et al. Thermal Ablation of… Fortschr Röntgenstr 2017; 189: 828–843

Review

Thi

s do

cum

ent w

as d

ownl

oade

d fo

r pe

rson

al u

se o

nly.

Una

utho

rized

dis

trib

utio

n is

str

ictly

pro

hibi

ted.

Page 14: Thermal Ablation of Lung Tumors: Focus on …...Thermal Ablation of Lung Tumors: Focus on Microwave Ablation Thermoablation von Lungentumoren: Mikrowellenablation im Fokus Authors

[19] Wei Z, Ye X, Yang X et al. Microwave ablation plus chemotherapy im-proved progression-free survival of advanced non-small cell lung cancercompared to chemotherapy alone. Medical oncology (Northwood, Lon-don, England) 2015; 32: 464

[20] Xu X, Ye X, Liu G et al. Targeted percutaneous microwave ablation at thepulmonary lesion combined with mediastinal radiotherapy with or with-out concurrent chemotherapy in locally advanced non-small cell lungcancer evaluation in a randomized comparison study. Medical oncology(Northwood, London, England) 2015; 32: 227

[21] Cheng M, Fay M, Steinke K. Percutaneous CT-guided thermal ablation assalvage therapy for recurrent non-small cell lung cancer after externalbeam radiotherapy: A retrospective study. International journal of hy-perthermia: the official journal of European Society for HyperthermicOncology, North American Hyperthermia Group 2016; 32: 316–323

[22] Egashira Y, Singh S, Bandula S et al. Percutaneous High-Energy Micro-wave Ablation for the Treatment of Pulmonary Tumors: A RetrospectiveSingle-Center Experience. Journal of vascular and interventional radiol-ogy: JVIR 2016; 27: 474–479

[23] Lubner MG, Brace CL, Hinshaw JL et al. Microwave tumor ablation:mechanism of action, clinical results, and devices. Journal of vascularand interventional radiology: JVIR 2010; 21: S192–S203

[24] Ward RC, Healey TT, Dupuy DE. Microwave ablation devices for inter-ventional oncology. Expert review of medical devices 2013; 10: 225–238

[25] Simo KA, Tsirline VB, Sindram D et al. Microwave ablation using 915-MHzand 2.45-GHz systems: what are the differences? HPB: the official jour-nal of the International Hepato Pancreato Biliary Association 2013; 15:991–996

[26] Goldberg SN. Radiofrequency tumor ablation: principles and tech-niques. European journal of ultrasound: official journal of the EuropeanFederation of Societies for Ultrasound in Medicine and Biology 2001; 13:129–147

[27] Vogl TJ, Naguib NN, Lehnert T et al. Radiofrequency, microwave andlaser ablation of pulmonary neoplasms: clinical studies and technicalconsiderations–review article. European journal of radiology 2011; 77:346–357

[28] Hinshaw JL, Lubner MG, Ziemlewicz TJ et al. Percutaneous tumor abla-tion tools: microwave, radiofrequency, or cryoablation–what should youuse and why? Radiographics: a review publication of the RadiologicalSociety of North America, Inc 2014; 34: 1344–1362

[29] Koizumi T, Tsushima K, Tanabe T et al. Bronchoscopy-Guided CooledRadiofrequency Ablation as a Novel Intervention Therapy for PeripheralLung Cancer. Respiration; international review of thoracic diseases 2015;90: 47–55

[30] Alexander ES, Dupuy DE. Lung cancer ablation: technologies and tech-niques. Seminars in interventional radiology 2013; 30: 141–150

[31] McDevitt JL, Mouli SK, Nemcek AA et al. Percutaneous Cryoablation forthe Treatment of Primary and Metastatic Lung Tumors: Identification ofRisk Factors for Recurrence and Major Complications. Journal of vascularand interventional radiology: JVIR 2016; 27: 1371–1379

[32] Savic LJ, Chapiro J, Hamm B et al. Irreversible Electroporation in Inter-ventional Oncology: Where We Stand and Where We Go. RoFo: For-tschritte auf dem Gebiete der Rontgenstrahlen und der Nuklearmedizin2016; 188: 735–745

[33] Brace CL, Hinshaw JL, Laeseke PF et al. Pulmonary thermal ablation:comparison of radiofrequency and microwave devices by using grosspathologic and CT findings in a swine model. Radiology 2009; 251:705–711

[34] Andreano A, Huang Y, Meloni MF et al. Microwaves create larger abla-tions than radiofrequency when controlled for power in ex vivo tissue.Medical physics 2010; 37: 2967–2973

[35] Steinke K, Haghighi KS, Wulf S et al. Effect of vessel diameter on thecreation of ovine lung radiofrequency lesions in vivo: preliminary results.The Journal of surgical research 2005; 124: 85–91

[36] Gillams AR, Lees WR. Radiofrequency ablation of lung metastases:factors influencing success. European radiology 2008; 18: 672–677

[37] Planche O, Teriitehau C, Boudabous S et al. In vivo evaluation of lungmicrowave ablation in a porcine tumor mimic model. Cardiovascular andinterventional radiology 2013; 36: 221–228

[38] Crocetti L, Bozzi E, Faviana P et al. Thermal ablation of lung tissue: in vivoexperimental comparison of microwave and radiofrequency. Cardiovas-cular and interventional radiology 2010; 33: 818–827

[39] Alonzo M, Bos A, Bennett S et al. The Emprint Ablation System withThermosphere Technology: One of the Newer Next-Generation Micro-wave Ablation Technologies. Seminars in interventional radiology 2015;32: 335–338

[40] Hoffmann R, Rempp H, Erhard L et al. Comparison of four microwaveablation devices: an experimental study in ex vivo bovine liver. Radiology2013; 268: 89–97

[41] Patel IJ, Davidson JC, Nikolic B et al. Consensus guidelines for periproce-dural management of coagulation status and hemostasis risk in percu-taneous image-guided interventions. Journal of vascular and interven-tional radiology: JVIR 2012; 23: 727–736

[42] Hoffmann RT, Jakobs TF, Lubienski A et al. Percutaneous radiofrequencyablation of pulmonary tumors–is there a difference between treatmentunder general anaesthesia and under conscious sedation? Europeanjournal of radiology 2006; 59: 168–174

[43] Smith SL, Jennings PE. Lung radiofrequency and microwave ablation: areview of indications, techniques and post-procedural imaging appear-ances. Br J Radiol 2015; 88: DOI: 20140598

[44] Lal H, Neyaz Z, Nath A et al. CT-Guided Percutaneous Biopsy of Intra-thoracic Lesions. Korean Journal of Radiology 2012; 13: 210–226

[45] Swischuk JL, Castaneda F, Patel JC et al. Percutaneous transthoracicneedle biopsy of the lung: review of 612 lesions. Journal of vascular andinterventional radiology: JVIR 1998; 9: 347–352

[46] Charig MJ, Phillips AJ. CT-guided cutting needle biopsy of lung lesions–safety and efficacy of an out-patient service. Clinical radiology 2000; 55:964–969

[47] Kazerooni EA, Lim FT, Mikhail A et al. Risk of pneumothorax in CT-guidedtransthoracic needle aspiration biopsy of the lung. Radiology 1996; 198:371–375

[48] Kim Y-s, Lee WJ, Rhim H et al. The Minimal Ablative Margin of Radiofre-quency Ablation of Hepatocellular Carcinoma (> 2 and < 5 cm) Neededto Prevent Local Tumor Progression: 3D Quantitative Assessment UsingCT Image Fusion. American Journal of Roentgenology 2010; 195: 758–765

[49] Wang X, Sofocleous CT, Erinjeri JP et al. Margin size is an independentpredictor of local tumor progression after ablation of colon cancer livermetastases. Cardiovascular and interventional radiology 2013; 36: 166–175

[50] Anderson EM, Lees WR, Gillams AR. Early indicators of treatment successafter percutaneous radiofrequency of pulmonary tumors. Cardiovascu-lar and interventional radiology 2009; 32: 478–483

[51] de Baere T, Palussiere J, Auperin A et al. Midterm local efficacy and sur-vival after radiofrequency ablation of lung tumors with minimum follow-up of 1 year: prospective evaluation. Radiology 2006; 240: 587–596

[52] Giraud P, Antoine M, Larrouy A et al. Evaluation of microscopic tumorextension in non-small-cell lung cancer for three-dimensional conformalradiotherapy planning. International journal of radiation oncology, biol-ogy, physics 2000; 48: 1015–1024

[53] Hiraki T, Mimura H, Gobara H et al. Two cases of needle-tract seedingafter percutaneous radiofrequency ablation for lung cancer. Journal ofvascular and interventional radiology: JVIR 2009; 20: 415–418

841Vogl TJ et al. Thermal Ablation of… Fortschr Röntgenstr 2017; 189: 828–843

Thi

s do

cum

ent w

as d

ownl

oade

d fo

r pe

rson

al u

se o

nly.

Una

utho

rized

dis

trib

utio

n is

str

ictly

pro

hibi

ted.

Page 15: Thermal Ablation of Lung Tumors: Focus on …...Thermal Ablation of Lung Tumors: Focus on Microwave Ablation Thermoablation von Lungentumoren: Mikrowellenablation im Fokus Authors

[54] Hiraki T, Gobara H, Fujiwara H et al. Lung cancer ablation: complications.Seminars in interventional radiology 2013; 30: 169–175

[55] Abtin FG, Eradat J, Gutierrez AJ et al. Radiofrequency ablation of lungtumors: imaging features of the postablation zone. Radiographics 2012;32: 947–969

[56] Chheang S, Abtin F, Guteirrez A et al. Imaging Features following Ther-mal Ablation of Lung Malignancies. Seminars in interventional radiology2013; 30: 157–168

[57] Palussiere J, Marcet B, Descat E et al. Lung tumors treated with percuta-neous radiofrequency ablation: computed tomography imaging follow-up. Cardiovasc Intervent Radiol 2011; 34: 989–997

[58] Yamamoto A, Nakamura K, Matsuoka T et al. Radiofrequency ablation ina porcine lung model: correlation between CT and histopathologic find-ings. American journal of roentgenology 2005; 185: 1299–1306

[59] Miao Y, Ni Y, Bosmans H et al. Radiofrequency ablation for eradication ofpulmonary tumor in rabbits. The Journal of surgical research 2001; 99:265–271

[60] Goldberg SN, Grassi CJ, Cardella JF et al. Image-guided tumor ablation:standardization of terminology and reporting criteria. Journal of vascularand interventional radiology: JVIR 2009; 20: S377–S390

[61] Zaheer SN, Whitley JM, Thomas PA et al. Would you bet on PET? Evalua-tion of the significance of positive PET scan results post-microwaveablation for non-small cell lung cancer. Journal of medical imaging andradiation oncology 2015; 59: 702–712

[62] Steinke K, Glenn D, King J et al. Percutaneous imaging-guided radiofre-quency ablation in patients with colorectal pulmonary metastases:1-year follow-up. Annals of surgical oncology 2004; 11: 207–212

[63] Bojarski JD, Dupuy DE, Mayo-Smith WW. CT imaging findings of pulmo-nary neoplasms after treatment with radiofrequency ablation: results in32 tumors. American journal of roentgenology 2005; 185: 466–471

[64] Nour-Eldin NE, Naguib NN, Tawfik AM et al. CT volumetric assessment ofpulmonary neoplasms after radiofrequency ablation: when to consider asecond intervention? Journal of vascular and interventional radiology:JVIR 2014; 25: 347–354

[65] Suh RD, Wallace AB, Sheehan RE et al. Unresectable pulmonary malig-nancies: CT-guided percutaneous radiofrequency ablation–preliminaryresults. Radiology 2003; 229: 821–829

[66] Singnurkar A, Solomon SB, Gonen M et al. 18F-FDG PET/CT for the pre-diction and detection of local recurrence after radiofrequency ablationof malignant lung lesions. Journal of nuclear medicine: official publica-tion, Society of Nuclear Medicine 2010; 51: 1833–1840

[67] Deandreis D, Leboulleux S, Dromain C et al. Role of FDG PET/CT andchest CT in the follow-up of lung lesions treated with radiofrequencyablation. Radiology 2011; 258: 270–276

[68] Bonichon F, Palussiere J, Godbert Y et al. Diagnostic accuracy of 18F-FDGPET/CT for assessing response to radiofrequency ablation treatment inlung metastases: a multicentre prospective study. European journal ofnuclear medicine and molecular imaging 2013; 40: 1817–1827

[69] Sharma A, Lanuti M, He W et al. Increase in fluorodeoxyglucose positronemission tomography activity following complete radiofrequency abla-tion of lung tumors. Journal of computer assisted tomography 2013; 37:9–14

[70] Suzawa N, Yamakado K, Takao M et al. Detection of local tumor pro-gression by (18)F-FDG PET/CT following lung radiofrequency ablation:PET versus CT. Clinical nuclear medicine 2013; 38: e166–e170

[71] Sharma A, Digumarthy SR, Kalra MK et al. Reversible locoregional lymphnode enlargement after radiofrequency ablation of lung tumors. Amer-ican journal of roentgenology 2010; 194: 1250–1256

[72] Tsuda M, Rikimaru H, Majima K et al. Time-related changes of radiofre-quency ablation lesion in the normal rabbit liver: findings of magneticresonance imaging and histopathology. Investigative radiology 2003;38: 525–531

[73] Oyama Y, Nakamura K, Matsuoka T et al. Radiofrequency ablated lesionin the normal porcine lung: long-term follow-up with MRI and patholo-gy. Cardiovascular and interventional radiology 2005; 28: 346–353

[74] Gadaleta C, Mattioli V, Colucci G et al. Radiofrequency ablation of40 lung neoplasms: preliminary results. American journal of roentgen-ology 2004; 183: 361–368

[75] Okuma T, Matsuoka T, Yamamoto A et al. Assessment of early treatmentresponse after CT-guided radiofrequency ablation of unresectable lungtumours by diffusion-weighted MRI: a pilot study. The British journal ofradiology 2009; 82: 989–994

[76] Liu BD, Zhi XY. Expert consensus on image-guided radiofrequencyablation of pulmonary tumors-2015 edition. Translational lung cancerresearch 2015; 4: 310–321

[77] Matsui Y, Hiraki T, Gobara H et al. Phrenic nerve injury after radiofre-quency ablation of lung tumors: retrospective evaluation of the inci-dence and risk factors. Journal of vascular and interventional radiology:JVIR 2012; 23: 780–785

[78] Hiraki T, Gobara H, Mimura H et al. Brachial nerve injury caused by per-cutaneous radiofrequency ablation of apical lung cancer: a report of fourcases. Journal of vascular and interventional radiology: JVIR 2010; 21:1129–1133

[79] Yang X, Zhang K, Ye X et al. Artificial pneumothorax for pain relief duringmicrowave ablation of subpleural lung tumors. Indian journal of cancer2015; 52 (Suppl. 2): e80–e83

[80] de Baere T, Auperin A, Deschamps F et al. Radiofrequency ablation is avalid treatment option for lung metastases: experience in 566 patientswith 1037 metastases. Annals of oncology: official journal of the Euro-pean Society for Medical Oncology / ESMO 2015; 26: 987–991

[81] Hiraki T, Tajiri N, Mimura H et al. Pneumothorax, pleural effusion, andchest tube placement after radiofrequency ablation of lung tumors:incidence and risk factors. Radiology 2006; 241: 275–283

[82] Nour-Eldin NE, Naguib NN, Saeed AS et al. Risk factors involved in thedevelopment of pneumothorax during radiofrequency ablation of lungneoplasms. American journal of roentgenology 2009; 193: W43–W48

[83] Yoshimatsu R, Yamagami T, Terayama K et al. Delayed and recurrentpneumothorax after radiofrequency ablation of lung tumors. Chest2009; 135: 1002–1009

[84] Zheng A, Yang X, Ye X et al. Bronchopleural fistula after lung ablation:Experience in two cases and literature review. Indian journal of cancer2015; 52 (Suppl. 2): e41–e46

[85] Nour-Eldin NE, Naguib NN, Mack M et al. Pulmonary hemorrhage com-plicating radiofrequency ablation, from mild hemoptysis to life-threat-ening pattern. European radiology 2011; 21: 197–204

[86] Tajiri N, Hiraki T, Mimura H et al. Measurement of pleural temperatureduring radiofrequency ablation of lung tumors to investigate its rela-tionship to occurrence of pneumothorax or pleural effusion. Cardiovas-cular and interventional radiology 2008; 31: 581–586

[87] Kashima M, Yamakado K, Takaki H et al. Complications after 1000 lungradiofrequency ablation sessions in 420 patients: a single center's ex-periences. American journal of roentgenology 2011; 197: W576–W580

[88] Vansteenkiste J, De Ruysscher D, Eberhardt WE et al. Early and locallyadvanced non-small-cell lung cancer (NSCLC): ESMO Clinical PracticeGuidelines for diagnosis, treatment and follow-up. Annals of oncology:official journal of the European Society for Medical Oncology / ESMO2013; 24 (Suppl. 6): vi89–vi98

[89] Vansteenkiste J, Crino L, Dooms C et al. 2nd ESMO Consensus Confer-ence on Lung Cancer: early-stage non-small-cell lung cancer consensuson diagnosis, treatment and follow-up. Annals of oncology: official jour-nal of the European Society for Medical Oncology / ESMO 2014; 25:1462–1474

[90] Bi N, Shedden K, Zheng X et al. Comparison of the Effectiveness ofRadiofrequency Ablation With Stereotactic Body Radiation Therapy in

842 Vogl TJ et al. Thermal Ablation of… Fortschr Röntgenstr 2017; 189: 828–843

Review

Thi

s do

cum

ent w

as d

ownl

oade

d fo

r pe

rson

al u

se o

nly.

Una

utho

rized

dis

trib

utio

n is

str

ictly

pro

hibi

ted.

Page 16: Thermal Ablation of Lung Tumors: Focus on …...Thermal Ablation of Lung Tumors: Focus on Microwave Ablation Thermoablation von Lungentumoren: Mikrowellenablation im Fokus Authors

Inoperable Stage I Non-Small Cell Lung Cancer: A Systemic Review andPooled Analysis. International journal of radiation oncology, biology,physics 2016; 95: 1378–1390

[91] Dupuy DE, Fernando HC, Hillman S et al. Radiofrequency ablation ofstage IA non-small cell lung cancer in medically inoperable patients:Results from the American College of Surgeons Oncology Group Z4033(Alliance) trial. Cancer 2015; 121: 3491–3498

[92] Kwan SW, Mortell KE, Talenfeld AD et al. Thermal ablation matchessublobar resection outcomes in older patients with early-stage non-small cell lung cancer. Journal of vascular and interventional radiology:JVIR 2014; 25: 1–9.e1

[93] Leung VA, DiPetrillo TA, Dupuy DE. Image-guided tumor ablation for thetreatment of recurrent non-small cell lung cancer within the radiationfield. European journal of radiology 2011; 80: e491–e499

[94] Schoellnast H, Deodhar A, Hsu M et al. Recurrent non-small cell lungcancer: evaluation of CT-guided radiofrequency ablation as salvagetherapy. Acta radiologica (Stockholm, Sweden: 1987) 2012; 53: 893–899

[95] Ahmed M, Moussa M, Goldberg SN. Synergy in cancer treatment be-tween liposomal chemotherapeutics and thermal ablation. Chemistryand physics of lipids 2012; 165: 424–437

[96] Zhao Z, Su Z, Zhang W et al. A randomized study comparing the effec-tiveness of microwave ablation radioimmunotherapy and postoperativeadjuvant chemoradiation in the treatment of non-small cell lung cancer.Journal of BUON: official journal of the Balkan Union of Oncology 2016;21: 326–332

[97] Bastianpillai C, Petrides N, Shah T et al. Harnessing the immunomodula-tory effect of thermal and non-thermal ablative therapies for cancer

treatment. Tumour biology: the journal of the International Society forOncodevelopmental Biology and Medicine 2015; 36: 9137–9146

[98] Adkins I, Fucikova J, Garg AD et al. Physical modalities inducing immu-nogenic tumor cell death for cancer immunotherapy. Oncoimmunology2014; 3: DOI: e968434

[99] Chen DS, Mellman I. Oncology meets immunology: the cancer-immu-nity cycle. Immunity 2013; 39: 1–10

[100] Weiser MR, Jarnagin WR, Saltz LB. Colorectal cancer patients witholigometastatic liver disease: what is the optimal approach? Oncology(Williston Park, NY) 2013; 27: 1074–1078

[101] Van Cutsem E, Cervantes A, Adam R et al. ESMO consensus guidelinesfor the management of patients with metastatic colorectal cancer.Annals of oncology: official journal of the European Society for MedicalOncology / ESMO 2016; 27: 1386–1422

[102] Rieber J, Streblow J, Uhlmann L et al. Stereotactic body radiotherapy(SBRT) for medically inoperable lung metastases-A pooled analysis ofthe German working group "stereotactic radiotherapy". Lung cancer(Amsterdam, Netherlands) 2016; 97: 51–58

[103] Lyons NJ, Pathak S, Daniels IR et al. Percutaneous management ofpulmonary metastases arising from colorectal cancer; a systematicreview. European journal of surgical oncology: the journal of theEuropean Society of Surgical Oncology and the British Associationof Surgical Oncology 2015; 41: 1447–1455

[104] Crombe A, Buy X, Godbert Y et al. 23 Lung Metastases Treated byRadiofrequency Ablation Over 10 Years in a Single Patient: SuccessfulOncological Outcome of a Metastatic Cancer Without Altered Respira-tory Function. Cardiovascular and interventional radiology 2016.DOI: 10.1007/s0027001614458

843Vogl TJ et al. Thermal Ablation of… Fortschr Röntgenstr 2017; 189: 828–843

Thi

s do

cum

ent w

as d

ownl

oade

d fo

r pe

rson

al u

se o

nly.

Una

utho

rized

dis

trib

utio

n is

str

ictly

pro

hibi

ted.